Review
Structure, gene expression, and putative functions of crustacean heat shock proteins in innate immunity

https://doi.org/10.1016/j.dci.2020.103875Get rights and content

Highlights

  • Review of the structure, expression, and putative function of heat shock proteins (HSPs) in crustacean innate immunity.

  • Summary of crustacean HSP responses to pathogens.

  • Presentation of the research progress on the regulation of immune-related genes by crustacean HSPs.

  • Proposal of a model for the HSP70-mediated enhancement of shrimp innate immunity.

Abstract

Heat shock proteins (HSPs) are molecular chaperones with critical roles in the maintenance of cellular proteostasis. HSPs, which regulate protein folding and refolding, assembly, translocation, and degradation, are induced in response to physiological and environmental stressors. In recent years, HSPs have been recognized for their potential role in immunity; in particular, these proteins elicit a variety of immune responses to infection and modulate inflammation. This review focuses on delineating the structural and functional roles of crustacean HSPs in the innate immune response. Members of crustacean HSPs include high molecular weight HSPs (HSP90, HSP70, and HSP60) and small molecular weight HSPs (HSP21 and HSP10). The sequences and structures of these HSPs are highly conserved across various crustacean species, indicating strong evolutionary links among this group of organisms. The expression of HSP-encoding genes across different crustacean species is significantly upregulated upon exposure to a wide range of pathogens, emphasizing the important role of HSPs in the immune response. Functional studies of crustacean HSPs, particularly HSP70s, have demonstrated their involvement in the activation of several immune pathways, including those mediating anti-bacterial resistance and combating viral infections, upon heat exposure. The immunomodulatory role of HSPs indicates their potential use as an immunostimulant to enhance shrimp health for control of disease in aquaculture.

Section snippets

General introduction

Heat shock proteins (HSPs) or molecular chaperones are evolutionarily conserved proteins found in the subcellular compartments (including the nucleus, endoplasmic reticulum (ER), cytosol, mitochondrion, and chloroplast) of all prokaryotic and eukaryotic cells (Hartl and Hayer-Hartl, 2002; Lindquist and Craig, 1988; Robert, 2003). In normal cells, HSPs represent 5–10% of the total protein content and are induced on exposure not only to heat but also to other physiological and environmental

Crustacean heat shock proteins

In crustaceans, the HSP family has a variety of functions that range from acting as stress proteins to serving as extrinsic chaperones, and includes the following principal members: HSP90, HSP70, HSP60, HSP21, and HSP10 (Yik Sung, 2013). In addition to being categorized with respect to their molecular weights, HSPs can also be classified according to their expression: i) HSPs that are commonly expressed constitutively, such as heat shock cognates (HSCs), or ii) HSPs whose expression is induced

Gene expression of crustacean HSPs in response to pathological stress

HSPs are also known as stress proteins because they are produced by cells in response to various stress conditions (Johnston et al., 2018). Environmental stresses such as thermal stress, heavy metal or free radical exposure, osmotic stress, desiccation, pathological stress, and other stressors can trigger the expression of HSPs to protect cells from damage (Srivastava, 2002; Yik Sung and MacRae, 2011). Herein, the expression of crustacean HSPs in response to pathological stress in different

The HSP70 family and its role in crustacean immunity

The HSP70 family comprises the most well-characterized HSPs. The induction of HSP70 expression could enhance crustacean immunity as shown after animals are exposed to heat stress. Shrimp (P. vannamei) exposed to chronic NLHS showed higher expression of LvHSP70, LvHSP90 and immune-related genes: LvproPO and LvCrustin (Junprung et al., 2017). The high expression of LvproPO and Hemocyanin was also observed in shrimp exposed with acute NLHS (Loc et al., 2013). Moreover, shrimp exposed to either

Summary and perspectives

It is evident that HSPs act not only as molecular chaperones involved in protein folding and degradation, but also as stimulators of the innate immune system in response to thermal stress and pathogenic infections. In crustaceans, HSPs, especially HSP70s, have been linked to immune stimulation, affording resistance to bacterial and viral infections. Crustaceans exposed to heat stress or supplemented with recombinant HSPs exhibit enhanced resistance to pathogens as a result of immune activation.

Funding

This work was supported by the Thailand Research Fund [International Research Network Scholar No. IRN61W0001], awarded to A.T. The authors would like to thank Chulalongkorn University for providing support under the Ratchadapisek Somphot Endowment Fund to the Center of Excellence for Molecular Biology and Genomic of Shrimp and for funding W.J.‘s postdoctoral fellowship.

References (158)

  • P. Bozaykut et al.

    Regulation of protein turnover by heat shock proteins

    Free Radic. Biol. Med.

    (2014)
  • K.L. Buchanan

    Stress and the evolution of condition-dependent signals

    Trends Ecol. Evol.

    (2000)
  • S. Carra et al.

    The growing world of small heat shock proteins: from structure to functions

    Cell Stress Chaperones

    (2017)
  • J. Chen et al.

    Regions outside the α-crystallin domain of the small heat shock protein Hsp26 are required for its dimerization

    J. Mol. Biol.

    (2010)
  • E.J. Cimino et al.

    A newly developed ELISA showing the effect of environmental stress on levels of hsp86 in Cherax quadricarinatus and Penaeus monodon

    Comp. Biochem. Physiol. Mol. Integr. Physiol.

    (2002)
  • K.F. Clark et al.

    Molecular immune response of the American lobster (Homarus americanus) to the white spot syndrome virus

    J. Invertebr. Pathol.

    (2013)
  • A. Clavero-Salas et al.

    Transcriptome analysis of gills from the white shrimp Litopenaeus vannamei infected with White spot syndrome virus

    Fish Shellfish Immunol.

    (2007)
  • M. Daugaard et al.

    The heat shock protein 70 family: highly homologous proteins with overlapping and distinct functions

    FEBS Lett.

    (2007)
  • C.W. Dong et al.

    Differential expression of three Paralichthys olivaceus Hsp40 genes in responses to virus infection and heat shock

    Fish Shellfish Immunol.

    (2006)
  • K.S. Elicker et al.

    Genome-wide analysis and expression profiling of the small heat shock proteins in zebrafish

    Gene

    (2007)
  • Y. Gai et al.

    The construction of a cDNA library enriched for immune genes and the analysis of 7535 ESTs from Chinese mitten crab Eriocheir sinensis

    Fish Shellfish Immunol.

    (2009)
  • Q. Gao et al.

    Molecular cloning, characterization and expression of heat shock protein 90 gene in the haemocytes of bay scallop Argopecten irradians

    Fish Shellfish Immunol.

    (2008)
  • Q. Ge et al.

    Transcriptome analysis of the hepatopancreas in Exopalaemon carinicauda infected with an AHPND-causing strain of Vibrio parahaemolyticus

    Fish Shellfish Immunol.

    (2017)
  • B. Hu et al.

    Bacterial HSP70 (DnaK) is an efficient immune stimulator in Litopenaeus vannamei

    Aquaculture

    (2014)
  • P.Y. Huang et al.

    Identification of the small heat shock protein, HSP21, of shrimp Penaeus monodon and the gene expression of HSP21 is inactivated after white spot syndrome virus (WSSV) infection

    Fish Shellfish Immunol.

    (2008)
  • C.R. Hunt et al.

    Characterization and expression of the mouse Hsc70 gene

    Biochim. Biophys. Acta Gene Struct. Expr.

    (1999)
  • M.T.M. Iryani et al.

    Knockdown of heat shock protein 70 (Hsp70) by RNAi reduces the tolerance of Artemia franciscana nauplii to heat and bacterial infection

    J. Exp. Mar. Biol. Ecol.

    (2017)
  • H.C. Jha et al.

    Chlamydia pneumoniae heat shock protein 60 is associated with apoptotic signaling pathway in human atheromatous plaques of coronary artery disease patients

    J. Cardiol.

    (2011)
  • J. Jiang et al.

    Structural basis of interdomain communication in the Hsc70 chaperone

    Mol. Cell.

    (2005)
  • G. Jiang et al.

    ArHsp40, a type 1 J-domain protein, is developmentally regulated and stress inducible in post-diapause Artemia franciscana

    Cell Stress Chaperones

    (2016)
  • C.L. Johnston et al.

    Using single-molecule approaches to understand the molecular mechanisms of heat-shock protein chaperone function

    J. Mol. Biol.

    (2018)
  • W. Junprung et al.

    HSP70 and HSP90 are involved in shrimp Penaeus vannamei tolerance to AHPND-causing strain of Vibrio parahaemolyticus after non-lethal heat shock

    Fish Shellfish Immunol.

    (2017)
  • W. Junprung et al.

    Litopenaeus vannamei heat shock protein 70 (LvHSP70) enhances resistance to a strain of Vibrio parahaemolyticus, which can cause acute hepatopancreatic necrosis disease (AHPND), by activating shrimp immunity

    Dev. Comp. Immunol.

    (2019)
  • H. Kan et al.

    Molecular control of phenoloxidase-induced melanin synthesis in an insect

    J. Biol. Chem.

    (2008)
  • W.L. Kelley

    The J-domain family and the recruitment of chaperone power

    Trends Biochem. Sci.

    (1998)
  • J.G. Kiang et al.

    Heat shock protein 70 kDa: molecular Biology, biochemistry, and physiology

    Pharmacol. Ther.

    (1998)
  • J.H. Leu et al.

    A model for apoptotic interaction between white spot syndrome virus and shrimp

    Fish Shellfish Immunol.

    (2013)
  • C.S. Li et al.

    Heat shock protein 20 from Procambarus clarkii is involved in the innate immune responses against microbial infection

    Dev. Comp. Immunol.

    (2020)
  • F. Li et al.

    Cloning of cytoplasmic heat shock protein 90 (FcHSP90) from Fenneropenaeus chinensis and its expression response to heat shock and hypoxia

    Cell Stress Chaperones

    (2009)
  • P. Li et al.

    Molecular cloning, mRNA expression, and characterization of HSP90 gene from Chinese mitten crab Eriocheir japonica sinensis

    Comp. Biochem. Physiol. B

    (2009)
  • S. Liu et al.

    Transcriptome analysis of mud crab (Scylla paramamosain) gills in response to Mud crab reovirus (MCRV)

    Fish Shellfish Immunol.

    (2017)
  • W. Liu et al.

    Proteomic analysis of differentially expressed proteins in hemolymph of Scylla serrata response to white spot syndrome virus infection

    Aquaculture

    (2011)
  • V. Lopez et al.

    Bacteriaal HSP70 (DnaK) and mammalian Hsp70 interact differently with lipid membranes

    Cell Stress Chaperones

    (2016)
  • D. Magen et al.

    Mitochondrial Hsp60 chaperonopathy causes an autosomal-recessive neurodegenerative disorder linked to brain hypomyelination and leukodystrophy

    Am. J. Hum. Genet.

    (2008)
  • B.A. Maralit et al.

    Differentially expressed genes in hemocytes of Litopenaeus vannamei challenged with Vibrio parahaemolyticus AHPND (VPAHPND) and VPAHPND toxin

    Fish Shellfish Immunol.

    (2018)
  • P. Mehlen et al.

    Small stress proteins as novel regulators of apoptosis: heat shock protein 27 blocks fas/apo-1- and staurosporine-induced cell death

    J. Biol. Chem.

    (1996)
  • C.V. Nicchitta

    Biochemical, cell biological and immunological issues surrounding the endoplasmic reticulum chaperone GRP94/gp96

    Curr. Opin. Immunol.

    (1998)
  • S. Pongsomboon et al.

    A cDNA microarray approach for analyzing transcriptional changes in Penaeus monodon after infection by pathogens

    Fish Shellfish Immunol.

    (2011)
  • A. Prapavorarat et al.

    Identification of genes expressed in response to yellow head virus infection in the black tiger shrimp, Penaeus monodon, by suppression subtractive hybridization

    Dev. Comp. Immunol.

    (2010)
  • Z. Qiu et al.

    Diversity, structure, and expression of the gene for p26, a small heat shock protein from Artemia

    Genomics

    (2006)
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